Natural selenium stress influences the changes of antibiotic resistome in seleniferous forest soils

Environmental Microbiome - Tập 17 Số 1 - 2022
Fangfang Wang1, Guoping Liu1, Fan Zhang2, Zong-Ming Li1, Xiaolin Yang1, Chaodong Yang2, Jianlin Shen3, Ji‐Zheng He4, B Larry Li5, Jianguo Zeng6
1College of Animal Science, Yangtze University, Jingzhou 434025, China
2College of Horticulture and Gardening, Yangtze University, Jingzhou 434025, Hubei, China
3Key Laboratory of Agro-Ecological Processes in the Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, 410125, China
4Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, Vic 3010, Australia
5Department of Botany and Plant Sciences, University of California, Riverside, CA, 92521-0124, USA
6College of Veterinary Medicine, Hunan Agricultural University, Changsha 410128, China

Tóm tắt

AbstractBackgroundMetal(loid)s can promote the spread and enrichment of antibiotic resistance genes (ARGs) in the environment through a co-selection effect. However, it remains unclear whether exposure of microorganisms to varying concentrations of selenium (Se), an essential but potentially deleterious metal(loid) to living organisms, can influence the migration and distribution of ARGs in forest soils.ResultsPrecisely 235 ARGs conferring resistance to seven classes of antibiotics were detected along a Se gradient (0.06–20.65 mg kg−1) across 24 forest soils. (flor)/(chlor)/(am)phenicol resistance genes were the most abundant in all samples. The total abundance of ARGs first increased and then decreased with an elevated available Se content threshold of 0.034 mg kg−1(P = 2E−05). A structural equation model revealed that the dominant mechanism through which Se indirectly influences the vertical migration of ARGs is by regulating the abundance of the bacterial community. In addition, the methylation of Se (mediated bytehB) and the repairing of DNA damages (mediated byruvBandrecG) were the dominant mechanisms involved in Se resistance in the forest soils. The co-occurrence network analysis revealed a significant correlated cluster between Se-resistance genes, MGEs and ARGs, suggesting the co-transfer potential.Lelliottia amnigenaYTB01 isolated from the soil was able to tolerate 50 μg mL−1ampicillin and 1000 mg kg−1sodium selenite, and harbored both Se resistant genes and ARGs in the genome.ConclusionsOur study demonstrated that the spread and enrichment of ARGs are enhanced under moderate Se pressure but inhibited under severe Se pressure in the forest soil (threshold at 0.034 mg kg−1available Se content). The data generated in this pilot study points to the potential health risk associated with Se contamination and its associated influence on ARGs distribution in soil.

Từ khóa


Tài liệu tham khảo

Zowawi HM, Harris PN, Roberts MJ, Tambyah PA, Schembri MA, Pezzani MD, et al. The emerging threat of multidrug-resistant Gram-negative bacteria in urology. Nat Rev Urol. 2015;1210:570–84.

Pamer EG. Resurrecting the intestinal microbiota to combat antibiotic-resistant pathogens. Science. 2016;3526285:535.

Fresia P, Antelo V, Salazar C, Gimenez M, D’Alessandro B, Afshinnekoo E, et al. Urban metagenomics uncover antibiotic resistance reservoirs in coastal beach and sewage waters. Microbiome. 2019;7:35.

Pruden A, Pei RT, Storteboom H, Carlson KH. Antibiotic resistance genes as emerging contaminants: studies in northern Colorado. Environ Sci Technol. 2006;4023:7445–50.

Aminov RI. Horizontal gene exchange in environmental microbiota. Front Microbiol. 2011;2:158.

Seiler C, Berendonk TU. Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front Microbiol. 2012;369:399.

Zhu YG, Johnson TA, Su JQ, Qiao M, Guo GX, Stedtfeld RD, et al. Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci USA. 2013;1109:3435–40.

Berg J, Thorsen MK, Holm PE, Jensen J, Nybroe O, Brandt KK. Cu exposure under field conditions coselects for antibiotic resistance as determined by a novel cultivation-independent bacterial community tolerance assay. Environ Sci Technol. 2010;4422:8724–8.

Sun W, Qian X, Gu J, Wang XJ, Zhang L, Guo AY. Mechanisms and effects of arsanilic acid on antibiotic resistance genes and microbial communities during pig manure digestion. Bioresour Technol. 2017;234:217–23.

Zhao X, Shen J-P, Zhang L-M, Du S, Hu H-W, He J-Z. Arsenic and cadmium as predominant factors shaping the distribution patterns of antibiotic resistance genes in polluted paddy soils. J Hazard Mater. 2020;389:121838.

Combs GF, Scott ML. Nutritional interrelationships of vitamin-E and selenium. Bioscience. 1977;277:467–73.

Nancharaiah YV, Lens PN. Ecology and biotechnology of selenium-respiring bacteria. Microbiol Mol Biol Rev. 2015;791:61–80.

Heider J, Bock A. Selenium metabolism in microorganisms. Adv Microb Physiol. 1993;35:71–109.

Bulteau AL, Chavatte L. Update on selenoprotein biosynthesis. Antioxid Redox Sign. 2015;2310:775–94.

Letavayova L, Vlasakova D, Vlckova V, Brozmanova J, Chovanec M. Rad52 has a role in the repair of sodium selenite-induced DNA damage in Saccharomyces cerevisiae. Mutat Res-Gen Tox En. 2008;6522:198–203.

Schiavon M, Ertani A, Parrasia S, Vecchia FD. Selenium accumulation and metabolism in algae. Aquat Toxicol. 2017;189:1–8.

Van Hoewyk D, Takahashi H, Inoue E, Hess A, Tamaoki M, Pilon-Smits EAH. Transcriptome analyses give insights into selenium-stress responses and selenium tolerance mechanisms in Arabidopsis. Physiol Plantarum. 2008;1322:236–53.

Bebien M, Lagniel G, Garin J, Touati D, Vermeglio A, Labarre J. Involvement of superoxide dismutases in the response of Escherichia coli to selenium oxides. J Bacteriol. 2002;1846:1556–64.

Miranda AT, Gonzalez MV, Gonzalez G, Vargas E, Campos-Garcia J, Cervantes C. Involvement of DNA helicases in chromate resistance by Pseudomonas aeruginosa PAO1. Mutat Res-Fund Mol Mech. 2005;5781–2:202–9.

Liu M, Turner RJ, Winstone TL, Saetre A, Brenzinger MD, Jickling G, Tari LW. Escherichia coli TehB requires S-adenosylmethionine as a cofactor to mediate tellurite resistance. J Bacteriol. 2000;182:6509–13.

Li Z, Tan J, Shao L, Dong X, Ye RD, Chen D. Selenium-mediated protection in reversing the sensitivity of bacterium to the bactericidal antibiotics. J Trace Elem Med Biol. 2017;41:23–31.

Li L-G, Xia Y, Zhang T. Co-occurrence of antibiotic and metal resistance genes revealed in complete genome collection. ISME J. 2017;113:651–62.

Kieliszek M. Selenium-fascinating microelement, properties and sources in food. Molecules. 2019;24:1298.

Rayman MP. Selenium and human health. Lancet. 2012;379:1256–68.

Zhang L, Song H, Guo Y, Fan B, Huang Y, Mao X, et al. Benefit-risk assessment of dietary selenium and its associated metals intake in China (2017–2019): is current selenium-rich agro-food safe enough? J Hazard Mater. 2020;398:123224.

Bermingham EN, Hesketh JE, Sinclair BR, Koolaard JP, Roy NC. Selenium-enriched foods are more effective at increasing glutathione peroxidase (GPx) activity compared with selenomethionine: a meta-analysis. Nutrients. 2014;610:4002–31.

Phiri FP, Ander EL, Bailey EH, Chilima B, Chilimba ADC, Gondwe J, et al. The risk of selenium deficiency in Malawi is large and varies over multiple spatial scales. Sci Rep-UK. 2019;9:6566.

Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MOA, Dantas G. The shared antibiotic resistome of soil bacteria and human pathogens. Science. 2012;337:1107–11.

Zhu J, Wang N, Li S, Li L, Su H, Liu C. Distribution and transport of selenium in Yutangba, China: impact of human activities. Sci Total Environ. 2008;3922–3:252–61.

Yu T, Hou WL, Hou QY, Ma WJ, Xia XQ, Li YT, et al. Safe utilization and zoning on natural selenium-rich land resources: a case study of the typical area in Enshi County. China Environ Geochem Hlth. 2020;429:2803–18.

García JB, Krachler M, Chen B, Shotyk W. Improved determination of selenium in plant and peat samples using hydride generation-atomic fluorescence spectrometry (HG-AFS). Anal Chim Acta. 2005;5342:255–61.

Wang FH, Qiao M, Su JQ, Chen Z, Zhou X, Zhu YG. High throughput profiling of antibiotic resistance genes in urban park soils with reclaimed water irrigation. Environ Sci Technol. 2014;4816:9079–85.

Yuan X, Qiang Z, Ben W, Zhu B, Qu J. Distribution, mass load and environmental impact of multiple-class pharmaceuticals in conventional and upgraded municipal wastewater treatment plants in East China. Environ Sci-Proc Imp. 2015;173:596–605.

Muziasari WI, Pitkanen LK, Sorum H, Stedtfeld RD, Tiedje JM, Virta M. The resistome of farmed fish feces contributes to the enrichment of antibiotic resistance genes in sediments below baltic sea fish farms. Front Microbiol. 2017;7:2137.

Schimel J, Balser TC, Wallenstein M. Microbial stress-response physiology and its implications for ecosystem function. Ecology. 2007;886:1386.

Han XM, Hu HW, Shi XZ, Wang JT, Han LL, Chen D, et al. Impacts of reclaimed water irrigation on soil antibiotic resistome in urban parks of Victoria, Australia. Environ Pollut. 2016;211:48–57.

Suzuki MT, Taylor LT, DeLong EF. Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5 ’-nuclease assays. Appl Environ Microb. 2000;6611:4605–14.

He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG, et al. Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ Microbiol. 2007;9:2364–74.

Ranjard L, Prigent-Combaret C, Favre-Bonte S, Monnez C, Nazaret S, Cournoyer B. Characterization of a novel selenium methyltransferase from freshwater bacteria showing strong similarities with the calicheamicin methyltransferase. Biochim Biophys Acta-Gene Struct Expr. 2004;16791:80–5.

Driscoll DM, Copeland PR. Mechanism and regulation of selenoprotein synthesis. Annu Rev Nutr. 2003;23:17–40.

Krafft T, Bowen A, Theis F, Macy JM. Cloning and sequencing of the genes encoding the periplasmic-cytochrome B-containing selenate reductase of Thauera selenatis. DNA Seq J DNA Seq Mapp. 2000;106:365–77.

Kuroda M, Yamashita M, Miwa E, Imao K, Fujimoto N, Ono H, et al. Molecular cloning and characterization of the srdBCA operon, encoding the respiratory selenate reductase complex, from the selenate-reducing Bacterium Bacillus selenatarsenatis SF-1. J Bacteriol. 2011;1939:2141–8.

Zhou JZ, Wu LY, Deng Y, Zhi XY, Jiang YH, Tu QC, et al. Reproducibility and quantitation of amplicon sequencing-based detection. ISME J. 2011;58:1303–13.

Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;75:335–6.

Washburne AD, Morton JT, Sanders J, McDonald D, Zhu QY, Oliverio AM, et al. Methods for phylogenetic analysis of microbiome data. Nat Microbiol. 2018;36:652–61.

Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26(19):2460–1. https://doi.org/10.1093/bioinformatics/btq461.

Chin CS, Peluso P, Sedlazeck FJ, Nattestad M, Concepcion GT, Clum A. Phased diploid genome assembly with single-molecule real-time sequencing. Nat Methods. 2016;13(12):1050–4.

Hackl T, Hedrich R, Schultz J, Förster F. Proovread: large-scale high-accuracy PacBio correction through iterative short read consensus. Bioinformatics. 2014;30(21):3004–11.

Denisov G, Walenz B, Halpern AL, Miller J, Axelrod N, Levy S. Consensus generation andvariant detection by Celera Assembler. Bioinformatics. 2008;24(8):1035–40.

Delcher AL, Harmon D, Kasif S, White O, Salzberg SL. Improved microbial gene identification with GLIMMER. Nucleic Acids Res. 1999;2723:4636–41.

Delcher AL, Bratke KA, Powers EC, Salzberg SL. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics. 2007;236:673–9.

Bagheri H, Dyer R, Severin AJ, Rajan H. Comprehensive Analysis of Non Redundant Protein Database. Off Biotechnol Publ. 2020;9.

Bairoch A, Apweiler R. The SWISS-PROT protein sequence data bank and its supplement TrEMBL in 1999. Nucleic Acids Res. 1999;27:49–54.

Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. Gene ontology: tool for the unification of biology. Nat Genet. 2000;251:25–9.

Cepas JH, Szklarczyk D, Heller D, Plaza AH, Forslund SK, Cook H, et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res. 2019;47(D1):D309–14.

Alcock BP, Raphenya AR, Lau TTY, Tsang KK, Bouchard M, Edalatmand A, et al. CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res. 2020;48(D1):D517–25.

Blin K, Shaw S, Steinke K, Villebro R, Ziemert N, Lee SY, et al. antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res. 2019;47:81–7.

Fong Y, Huang Y, Gilbert PB, Permar SR. chngpt: threshold regression model estimation and inference. BMC Bioinform. 2017;18:454.

Oksanen J, Blanchet FG, Kindt R, Legendre P, O'Hara RG, Simpson G, et al. vegan: community ecology package 2.5–7. Ordination methods, diversity analysis and other functions for community and vegetation ecologists. 2020.

Rosseel Y. lavaan: an R package for structural equation modeling. J Stat Softw. 2012;48(2):1–36.

Lefcheck JS. piecewiseSEM: piecewise structural equation modeling in R for ecology, evolution, and systematics. Methods Ecol Evol. 2015;7(5):573–9.

Revelle W. psych: procedures for personality and psychological research. Evanston: Northwestern University; 2018.

Bastian M, Heymann S, Jacomy M. Gephi: an open source software for exploring and manipulating networks. In: International AAAI conference on weblogs and social media. 2009.

Vaz-Moreira I, Nunes OC, Manaia CM. Bacterial diversity and antibiotic resistance in water habitats: searching the links with the human microbiome. Fems Microbiol Rev. 2014;384:761–78.

Li Y, Cao W, Liang S, Yamasaki S, Chen X, Shi L, et al. Metagenomic characterization of bacterial community and antibiotic resistance genes in representative ready-to-eat food in southern China. Sci Rep-UK. 2020;101:15175–15175.

Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV. Co-selection of antibiotic and metal resistance. Trends Microbiol. 2006;144:176–82.

Gullberg E, Albrecht LM, Karlsson C, Sandegren L, Andersson DI. Selection of a multidrug resistance plasmid by sublethal levels of antibiotics and heavy metals. MBio. 2014;5:e01918-e2014.

Seiler C, Berendonk TU. Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front Microbiol. 2012;3:399.

Hu H-W, Wang J-T, Li J, Shi X-Z, Ma Y-B, Chen D, et al. Long-term nickel contamination increases the occurrence of antibiotic resistance genes in agricultural soils. Environ Sci Technol. 2017;512:790–800.

Forsberg KJ, Patel S, Gibson MK, Lauber CL, Knight R, Fierer N, et al. Bacterial phylogeny structures soil resistomes across habitats. Nature. 2014;509:612-+.

Stolz JE, Basu P, Santini JM, Oremland RS. Arsenic and selenium in microbial metabolism. Annu Rev Microbiol. 2006;60:107–30.

Gillings MR, Gaze WH, Pruden A, Smalla K, Tiedje JM, Zhu YG. Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution. ISME J. 2015;96:1269–79.

Hasman H, Aarestrup FM. tcrB, a gene conferring transferable copper resistance in Enterococcus faecium: occurrence, transferability, and linkage to macrolide and glycopeptide resistance. Antimicrob Agents Chemother. 2002;465:1410–6.

Hasman H, Aarestrup FM. Relationship between copper, glycopeptide, and macrolide resistance among Enterococcus faecium strains isolated from pigs in Denmark between 1997 and 2003. Antimicrob Agents Chemother. 2005;491:454–6.

Stolz JF, Basu P, Oremland RS. Microbial transformation of elements: the case of arsenic and selenium. Int Microbiol. 2002;54:201.

Rosenfeld CE, Kenyon JA, James BR, Santelli CM. Selenium (IV, VI) reduction and tolerance by fungi in an oxic environment. Geobiology. 2017;15:441–52.

Dhanjal S, Singh AK, Cameotra SS. Global gene expression analysis of bacterial stress response to elevated concentrations of toxic metalloids—selenium and arsenic. Geomicrobiol J. 2014;316:480–92.